Acta Zoológica Mexicana (nueva serie) ISSN: 0065-1737 [email protected] Instituto de Ecología, A.C. México

JEREZ, ADRIANA; SÁNCHEZ-MARTÍNEZ, PAOLA MARÍA; GUERRA-FUENTES, RICARDO ARTURO EMBRYONIC SKULL DEVELOPMENT IN THE NEOTROPICAL VIVIPAROUS (: SCINCIDAE) Acta Zoológica Mexicana (nueva serie), vol. 31, núm. 3, diciembre, 2015, pp. 391-402 Instituto de Ecología, A.C. Xalapa, México

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EMBRYONIC SKULL DEVELOPMENT IN THE NEOTROPICAL VIVIPAROUS SKINK MABUYA (SQUAMATA: SCINCIDAE)

A JEREZ1, P M SÁNCHEZ-MARTÍNEZ2 & R A GUERRA-FUENTES2,3

1Departamento de Biología. Universidad Nacional de Colombia, Sede Bogotá, Bogotá, Colombia. Carrera 45 No 26-85, Bogotá, Cundinamarca, Colombia. 2Museu de Zoologia da Universidade de São Paulo, São Paulo, Brasil. Av. Nazaré 481, Ipiranga, 04263-000, São Paulo (SP), Brasil. ; 3

Recibido: 01/03/2015; aceptado: 09/10/2015

Jerez, A., Sánchez-Martínez, P. M. & Guerra-Fuentes, R. A. 2015. Jerez, A., Sánchez-Martínez, P. M. & Guerra-Fuentes, R. A. 2015. Embryonic skull development in the neotropical viviparous skink Desarrollo embrionario del cráneo en la lagartija vivípara Mabu- Mabuya (Squamata: Scincidae). Acta Zoológica Mexicana (n.s.), ya (Squamata: Scincidae). Acta Zoológica Mexicana (n.s.), 31(3): 31(3): 391-402. 391-402.

ABSTRACT. The systematics of the Americans of the RESUMEN. La sistemática del género Mabuya ha sido extensamente Mabuya have been extensively studied, with new arrangements based estudiada en América y se han propuesto varios arreglos taxonómicos on molecular analysis. However, the skeletal morphology, their de- con base en análisis moleculares. Sin embargo, aspectos relacionados velopment and ontogenetic variation have been poorly studied in this con la morfología del esqueleto, su desarrollo y variación ontogenéti- genus. We described the embryonic skull development of three species ca han sido probrementente estudiados en este género. En el presente of Mabuya and compare it with the African species cap- trabajo se describe el desarrollo embrionario del cráneo en tres espe- ensis. We observed that American genus Mabuya presents differences cies del género Mabuya y se compara con el de la especie africana in the skull development, including the pila antotica, orbitosphenoid, Trachylepis capensis. Se encontró que el género Mabuya presenta di- vomer, and the basicranial fenestra closure. These morphological dif- ferencias en el desarrollo del cráneo respecto a la especie africana, ferences in Mabuya species may be interpreted as putative synapomor- incluyendo la pila antótica, el orbitosfenoides, el vómer, y el cierre de phic characters. la fenestra basicraneal. Estas diferencias en el desarrollo del cráneo Key words: Skull development, chondrocranium, Mabuya, skin, Scin- son importantes, ya que su presencia en todo el género Mabuya sugiere cidae, Squamata que se podría tratar de sinapomorfias para este clado. Palabras clave: Desarrollo craneal, condrocráneo, Mabuya, Scinci- dae, Squamata

INTRODUCTION posal and all species in this work are regarded to the ge- nus Mabuya. The genus Mabuya constitutes a monophyletic unit with a All Mabuya species present viviparous reproduction, recent diversification, and exhibits a unique combination smooth scales, lower eyelid with a semi-transparent disc, of reproductive features in Squamata (Blackburn & Vitt pterygoid teeth absent, and 25-31 presacral vertebrae 1992; Mausfeld et al. 2002; Carranza & Arnold 2003; (Mausfeld et al. 2002). This genus inhabits mainly low- Whiting et al. 2006; Miralles & Carranza 2010). land forests and evolved with a group of specializations Until recently, the pantropical genus Mabuya includ- related to viviparity, which are unique among and ed more than a hundred species distributed in America, convergent only with placental mammals: a long period and (Greer & Nussbaum 2000; Greer et al. of gestation (9 to 12 months) and microlecithal eggs (0.9- 2000). However, on the basis of a molecular phylogenetic 2.2 mm) with a highly placentotrophic nutritional pat- analysis this genus was divided into four clades (Maus- tern (Blackburn & Vitt 1992; Blackburn 1993; Jerez & feld et al. 2002). In this way, the genus Mabuya actually Ramírez 2001, 2003). includes about 53 species, distributed from Mexico to Ar- Despite the recent phylogenetic and taxonomic in- gentina (Ávila-Pires 1995; Mausfeld et al. 2002; Miralles terest in the evolution of the genus Mabuya (Mausfeld et al. 2005). The other three clades are Trachylepis (Fitz- et al. 2002; Carranza & Arnold 2003; Jesus et al. 2005; inger 1843) in Africa, (Gray 1845) in Cape Miralles et al. 2005; Whiting et al. 2006; Miralles et al. Verde, and (Fitzinger 1843) in Asia (Mausfeld 2009; Miralles & Carranza 2010; Hedges & Conn 2012), et al. 2002; Bauer 2003). We follow this taxonomic pro- osteological and ontogenetic descriptions in comparative 392 Jerez et al.: Skull development in Mabuya studies are scarce. Regarding African species, Skinner Mabuya sp. was compared with that of M. cassaira and (1973) described the ontogenetic and adult morphology in M. macrorhyncha, two Brazilian species. We described Trachylepis capensis skull, whereas Rao & Ramaswami a series of eight embryos of M. cassaira from Bertioga, (1952) described the fully formed chondrocranium and SP Brazil (MZUSP-40720, MZUSP-40771, MZUSP- the adult osteocranium of the Asian Eutropis carinata. 40777, MZUSP-40779, MZUSP-45703), and five of M. Concerning American species, Jerez (2012) described the macrorhyncha from Guarujá, SP, Brazil (MZUSP-40695, adult skull of Colombian Andean population of Mabuya MZUSP-40792, MZUSP 40800) and Ilha dos Búzios, SP, sp., and Caicedo (2012) analyzed the adult skull in differ- Brazil (MZUSP-11148, MZUSP 11176). In this compari- ent species and populations in Colombia. son we described embryos of stages 32, 39 and 40 (D&H) Hence, the main purpose of this work is to describe the for all species. The stage 34 (D&H) is described just for development of the embryonic skull in Mabuya sp., M. Mabuya sp. The skeletal embryonic development was cassaira and M. macrorhyncha. In addition, the chondro- described using cleared and double-stained specimens, cranium of Mabuya is compared with the species of the prepared following Wassersug (1976). The description of Trachylepis capensis and Eutropis carinata, the chondrocranium follows those of Bellairs & Kamal therefore, these morphological studies could provide ad- (1981). In Mabuya sp. the first stage is described, while ditional anatomical characters to support the taxonomic in the subsequent stages only the registered variations are status of this American clade as monophyletic. This is explained. In contrast, with M. caissara and M. macro- particularly important, given that Hedges & Conn (2012) rhyncha only the differences relating to Mabuya sp. are proposed sixteen genera for America. On the other hand, reported. though many molecular phylogenetic analyses support the monophyly of American clade (Mausfeld et al. 2002; Carranza & Arnold 2003; Jesus et al. 2005; Whiting et RESULTS al. 2006; Miralles & Carranza 2010), some herpetologists consider that the division of pantropical genus Mabuya in Mabuya sp. Stage 32-33 (Fig. 1): In this stage, elements four genera has been premature (Jesus et al. 2005; Whit- of three regions of the chondrocranium are observed: the ing et al. 2006). anterior ethmoidal region, the intermediate orbitotempo- ral region, and the posterior occipital region (Table 1). In the ethmoidal region, the cartilages of the nasal capsule MATERIALS AND METHODS start being condensed. The interorbital septum is low and contacts the trabecula communis. In the posterior region, We described the skull development in an Andean popu- the skull consists of the basal plate and the occipital arch. lation of Mabuya sp. and compared it with the transan- The elements of splachnocranium, the quadrate, the as- dean species M. caissara and M. macrorhycha. Mabuya is cending process and the Meckel´s cartilage are observed widely distributed in Colombia (Sánchez et al. 1995) and their populations represent a complex of species (Ávila- Pires 1995; Miralles et al. 2005; Miralles 2006). According to Miralles (2005) neither M. mabouya nor M. nigropunc- tata, nominations for populations in Colombia, are pres- ent in the Andean Colombian regions. For this reason, in this work the studied population is referred as Mabuya sp. The embryos of Mabuya sp. were taken from females of a population collected at the Inspección de Policía Guadu- alito, in the Municipality of Yacopí, Cundinamarca, Co- lombia. They are housed in the Colección Herpetologica, Escuela de Biología, Universidad Industrial de Santander. A series of twelve embryos of Mabuya sp. was selected (UIS-R-289, 310, 311, 314, 319, 320, 321, 351, 355, 366, 404, and 415). Stages of development follow Defaure & Hubert (1961), this table starts at stage 1 with the cleav- Figure 1. Chondrocranium of Mabuya sp. at stage 32-33 (D&H). Abbreviations: asp, ascending process; atl, atlas; axi, axis; age and ends at stage 40 with the hatching. The series bpl, basal plate; mc: Meckel cartilage; nc, nasal capsule; oca, studied include embryos from limb bud stage (stage 32) occipital region; ors, interorbital septum; pt, pterygoid; q, quadrate; to preparturition stage (stage 40). The chondrocranium of tc, trabecula communis. Scale bar: 1 mm. Acta Zool. Mex. (n.s.) 31(3) (2015) 393

Table 1. Major events of the skull development in three species of the Neotropical genus Mabuya. (Ms: Mabuya sp., Mm: M. macrorhyncha, Mc: M. caissara). Stages 32 34 39 40 Preparturition Species Ms Mm Mc Ms Mm Mc Ms Mm Mc Ms Mm Mc Ms Mm Mc Chondrocranium Nasal cartilages XXX Interobital septum XXX Trabecula comunis XXX Basal plate XXX Occipital arch XXX Capsula otica XX X

Sphenethmoid commissures XXX Fenestra olfactoria XXX High interorbital septum XXX Nasal septum XXX Taenia medialis, pila metoptica, XXX pila accessoria Pila antotica does not contact the XXX basal plate Basicranial fenestra XXX

Pariotectal and paranasal cartilages XXX Fenestra superior XXX Bifid maxillary process XXX Planum antorbitale XXX Planum supraseptale XXX Basicranial fenestra XXX Pituitary fenestra XXX

Basicranial fenestra small XXX Pituitary fenestra small XXX

Orbitosphenoid XXX Basicranial fenestrae closed or XXX almost closed Fenestrae pituitary closed XXX

(Table 1). The Meckel´s cartilages are fused at the sym- Differences to Mabuya caissara: There are no differ- phisis and caudally the retroarticular process is present. ences with this species (Table 1). Regarding to the dermatocranium, the pterygoid starts to Mabuya sp. Stage 34 (Fig. 2): In this stage the chondro- ossify (Table 2). cranium presents further development in orbitotemporal Differences with Mabuya macrorhyncha: in this stage and occipital regions (Table 1). In the orbitotemporal the cartilages of ethmoidal and orbitotemporal regions are region, the sphenethmoid commissures, a pair of arched not clearly observed in the chondrocranium. However, slender cartilaginous rods, extends from the nasal capsule the trabecula communis, the basal plate, the otic capsule to the planum supraseptale. Then it forms a large fenestra and the occipital arch are totally visible (Table 1). In the olfactoria. dermatocranium, besides the pterygoid, the dentary starts The interorbital septum has increased in height and to ossify in the anterior region of Meckel’s cartilage. appears continuously with the trabecula communis and 394 Jerez et al.: Skull development in Mabuya

Table 2. Ossification sequence of the skull in three species of the Neotropical genus Mabuya. (Ms: Mabuya sp., Mm: M. macrorhyncha, Mc: M. caissara). Stages 32 34 39 40 Preparturition Species Ms Mm Mc Ms Mm Mc Ms Mm Mc Ms Mm Mc Ms Mm Mc Ossification sequence Pterygoid X X X Dentary X X Prefrontal X X X Frontal X X X Parietal X X X Supratemporal X X X Palatine X X X Surangular X X X Premaxilla X X X Maxilla X X X Nasal X X X Jugal X X X Posfrontal X X X Postorbital X X X Squamosal X X X Supratemporal X X X Vomer X X X Palatine X X X Ectopterygoid X X X Epipterygoid X X X Manbible X X X Basisphenoid X X X Parasphenoid X X X Basioccipital X X X Exoccipital X X X Prootico XXX Ophistotic XXX Frontoparietal fenestra small XXX Orbitosphenoid XXX extends into the ethmoidal region of the chondrocranium the tectum synoticum is observed. In this stage, the basi- shaping of the nasal septum. Furthermore, the interorbital cranial fenestra is small and separated from the pituitary septum begins to develop other cartilages from the orbito- fossa by the crista sellaris. temporal scaffolding. The taenia medialis, the pila metop- In relation to the dermatocranium, other bony elements tica and the pila antotica are continuous cartilaginous start to ossify; these include the prefrontal, the frontal, the rods. Further behind, the pila accessoria extends between parietal, the supratemporal, the palatine, the dentary and the taenia marginalis and the pila antotica. This last one the surangular (Table 2). cartilage doesn’t contact the basal plate. The taenia mar- Mabuya sp. Stage 39 (Figs. 3, 4): In this stage the chon- ginalis extends between the pila accessoria and the dor- drocranium shows the configuration observed in the neo- sal surface of the otic capsule. In the occipital region, the nate. The principal changes are observed in the ethmoidal otic capsule is very conspicuous and presents the crista region, since the nasal cartilages are completely devel- parotica. In this posterior region, the skull roof is formed oped. The nasal capsule exhibits the pariotectal and para- by growth of the occipital arch and the otic capsule, then nasal cartilages (Table 1). Acta Zool. Mex. (n.s.) 31(3) (2015) 395

In the nasal region, the pariotectal cartilage presents de nasal cupola with the foramen apical and the narina. Posteriorly, the fenestra superior is very conspicuous dor- sally. The paranasal cartilage exhibits the bifid maxillary process, and the planum antorbitale, which is perpendicu- lar to nasal septum, but they are not in contact. In the orbitotemporal region, the planum supraseptale is completely formed; rostraly is formed by a cartilagi- nous rod and caudally by a width cartilaginous shield with a short process in the anterior region. The interorbital sep- tum presents the small anterior and ventral fenestra and the big posterior fenestra below the planum supraseptale. In this stage, the taenia marginalis extends from the planum supraseptale to the otic capsule. So the interobital scaf- folding is completely formed with all present cartilages. The epiotic fenestra is closed by the taenia marginalis, the taenia medialis, the pila metoptica and the pila accessoria. Figure 2. Chondrocranium of Mabuya sp. at stage 34 (D&H). On the other hand, the optic fenestra is closed by the pila Abbreviations: ce, sphenethmoid commisure; is, interorbital septum; metoptica and the interorbital septum. Finally, the fenes- f, frontal; mc, Meckel cartilage; nc, nasal capsule; cp, crista parotica; tra prootica and metoptica are continuous because the pila oc, occipital arch; oca, occipital region ; p, parietal; pac, pila antotica does not have contact with the basal plate. accesoria; pia, pila antotica; pim, pila metoptica; pfr, prefrontal; pls, In the occipital region, the otic capsule presents the planum supraseptale; pt, pterygoid; pof, ; q, quadrate ; pal, palatine ; rb, ribs; st,;tc, trabecula communis; tma, taenia marginalis; tme, fenestra ovalis, and the tectum synoticum exhibits the as- taenia medialis :ver: vertebrae. 1. Fenestra epióptica, 2. Fenestra cending process. Ventrally, the basipterygoid process is optica, 3. Fenestra prootica, 4. Fenestra metoptica. Scale bar: 1 mm. lengthy with the distal portion expanded and contacting

Figure 3. Chondrocranium of Mabuya sp. at stage 39 (D&H). (A) Lateral view, (B) Dorsal view. Abbreviations: afe, anterior fenestra; apr, anterior process; bpl, basal plate; c, nasal cupola; ec, esphenethomoid commisure; ef, foramen ephiphaniale; pm, maxillary process; pac, pila accessoria ; pfe, posterior fenestra; pia, pila antotica; pic, pariotectal cartilage; pim, pila metoptica; pla, planum antorbitale; pls, planum supraseptale; pnc, paranasal cartilage; q, quadrate; st, tectum synoticum; t, trabeculae; tma, taenis marginalis; tme, taenia medialis; vfe, ventral fenestra. 1. Fenestra epioptica, 2. Fenestra optica, 3. Fenestra prootica, 4. Fenestra metoptica. Scale bar: 1 mm. 396 Jerez et al.: Skull development in Mabuya

Figure 4. Dermatocranium of Mabuya sp. at stage 39 (D&H). (A) Dorsal View, (B) Ventral view. Abbreviations: asp, ascending process; bfe, basicranial fenestra; bpl, basal plate; bpp, basipterygoid process ; cb, basicapsular commisure; cl, columella; cs, crista sellaris; ept, ectopterygoid; exc, extra-columella; f, frontal; hf, hypoglossal foramen; m, maxilla; n, nasal; l, lacrimal; mf, fissura metotica; noc, notochord; p, parietal; pm, premaxilla; ps, parasphenoid; pt, pterygoid; pal, palatine; pfe, pituitary fenestra; pfo, perilymphatic foramen; pof, posfrontal; poo, postorbital; sq, squamosal; st, supratemporal; t, tectum synoticum; v, vomer; y, jugal. Scale bar: 1 mm. the pterygoid. The crista sellaris is a cartilaginous bar that 1). The fenestra lateralis is present in paranasal cartilage separates the pituitary fenestra and the basicranial fenes- of the nasal capsule, and the anterior process of the pla- tra. This last fenestra is small in this stage. Posteriorly, the num supraseptale is shorter and thicker. The ossification fissura metotica is separating the basal plate and the otic is observed in the medial and posterior regions of the bas- capsule. The perilymphatic foramen is present. al plate, which correspond to basisphenoid, basioccipital In this stage, ossification is beginning in the chondro- and exoccipital. cranium. The basisphenoid begins to ossify in the proximal Differences to Mabuya caissara: this species differs region of basipterygoid processes and the crista sellaris to the others species in the nasal capsule, exhibiting a (Table 2). Moreover, the parasphenoid is beginning to be short rostral process and lacking the anterior process of observed in the region of the pituitary fenestra. the planum supraseptale in this stage. However, this spe- Regarding splachnocranium, the quadrate is fully dif- cies is similar to Mabuya sp. in the other characteristics of ferentiated and appears ossified in the medial region. The the nasal and orbital region (Table 1). Regarding splach- ascending process has begun to ossify in the middle to nocranium, the columella is beginning the ossification. In form the epipterygoid bone. Meckel’s cartilage has be- this stage, the ossification of otic capsule, occipital arch come covered by the membrane bone of the lower jaw. and basal plate is more advanced than Mabuya sp. and M. Regarding dermatocranium, in this stage all dermal macrorhyncha. bones are present (Table 2). The bony elements of tem- Mabuya sp. Stage 40 (Figs. 7, 8): In this stage the princi- poral arch, palatine region and lower jaw are fully devel- pal change is the advanced ossification of the whole skull. oped, while the bone elements of nasal and orbital regions In the chondrocranium this is observed in the occipital are still being developed. This is remarkable in the frontal and supraoccipital region; the prootic, otoccipital (opis- and parietal bone since only the lateral edges are present. thotic-exoccipital), basioccipital and basisphenoid are Differences to Mabuya macrorhyncha (Figs. 5, 6): the present. The parasphenoid is a triradial bone observed in two species are very similar in their chondrocranium, al- the anterior region of the pituitary fenestra. The basicra- though there are slight differences between them (Table nial fenestra is smaller and it is limited by the basisphe- Acta Zool. Mex. (n.s.) 31(3) (2015) 397

Figure 5. Chondrocranium of M. macrorhycha at stage 39 (D&H). (A) Lateral view, (B) Dorsal view. Scale bar: 1 mm.

Figure 6. Dermatocranium of M. macrorhyncha at stage 39 (D&H). (A) Dorsal View, (B) Ventral view. Scale bar: 1 mm. 398 Jerez et al.: Skull development in Mabuya

Figure 7. Dermatocranium of Mabuya sp. at stage 40 (D&H). (A) Dorsal view, (B) Ventral view. Abbreviations: bo, basioccipital; bs, basisphenoid; bfe, basicranial fenestra; ces, quadrate ; epi II, epibranchial II; ps, parasphenoid; per, perilymphatic foramen; pro, prootico; otc, otoccipital otc; so, supraoccipital. Scale bar: 1 mm.

Figure 8. Dermatocranium of Mabuya sp. at stage 40, close to hatching. (A) Dorsal view, (B) Ventral view. Abbreviations: f,frontal; ffp, frontoparietal fenestra; ore, orbitosphenoid; ps, parabasisphenoid. Scale bar: 1 mm. Acta Zool. Mex. (n.s.) 31(3) (2015) 399 noid and basioccipital. The paroccipital process is formed Differences to Mabuya macrorhyncha and M. cais- by ossification of the crista parotica. The prootic presents sara (Fig. 9): the only difference is observed in embryos the alar process, which is projecting towards the epiptery- in preparturition stage, where the basicranial fenestra is goids, but does not contact this bone. Regarding derma- not completely closed (Table 1). tocranium, all bony elements are notably more developed than the stage before except of the frontal and parietal. Consequently, the frontoparietal fenestra is present. In the DISCUSSION lower jaw, all bone elements are completely developed. Embryos in preparturition stage present minimal In general, Mabuya species included in this morpho- changes (Fig. 8). In the orbitotemporal region of chondro- logical study exhibit a complete chondrocranium, with cranium, the orbitosphenoid is observed (Table 1). This is the ethmoidal, orbitotemporal and occipital regions ful- a semilunar ossification developed on the pila metotica. ly developed (Rao & Ramaswami 1952; Skinner 1973; In the occipital region, the parabasisphenoid is formed by Bellaris & Kamal 1981). In the ethmoidal region, the the fusion of basisphenoid and parasphenoid elements. nasal capsule of the Mabuya is broad, very developed, Finally, the basicranial and pituitary fenestrae are closed and similar to others lizards such as the scincids Chal- (Table 1). cides ocellatus, Eutropis carinata ( = Mabuya carinata), In the dermatocranium, frontal bones are not fully dif- Plestiodon fasciauts ( = Eumeces quinquelineatus), Tra- ferentiated in its posterior region yet. However, they are chylepis capensis ( = Mabuya capensis), Lygosoma, the fused in the medial region. The parietal is completely dif- lacertids Lacerta vivipara, and Acanthodactylus boski- ferentiated except in the anterior region. Therefore, the ana, the anguid Anguis fragilis, and the gimnophthalmid frontoparietal suture is not formed and the frontoparietal Ptychoglossus bicolor (Rice 1920; Pearson 1921; Rao fenestra is still present. This fenestra is smaller and ex- & Ramaswami 1952; El Toubi & Kamal 1961; Skinner tends as far out as the parietal foramen. 1973; Bellaris & Kamal 1981; Hernandez et al. 2012).

Figure 9. Dermatocranium of M. macrorhyncha at stage 40 (D&H). (A) Dorsal View, (B) Ventral view. Scale bar: 1 mm. 400 Jerez et al.: Skull development in Mabuya

The ethmoidal region in Mabuya species shares a num- in Mabuya species shows differences in the rate of ossifi- ber of common characteristics with others skinks (Bel- cation in respect to African and Asiatic species. laris & Kamal 1981); these species exhibit a large fenestra Regarding the ossification of chondrocranium (Table superior in the nasal capsule (Table 1), and the fenestra 2), in Mabuya species, it starts in stage 39 (D&H); af- lateralis is absent or small. In addition, Mabuya species, ter that, all elements of chondrocranium are ossified and like others skinks (C. ocellatus, E. carinata, P. fasciauts, joined by synchondrosis (stage 40 D&H). This condition T. capensis, Lygosoma) present a large fenestra olfacto- is observed in general in lizards, e.g. Trachylepis capen- ria (Rice 1920; Pearson 1921; Rao & Ramaswami 1952; sis, Elgaria coerulea, Liolaemus scapularis and Ptycho- Skinner 1973; Bellaris & Kamal 1981). This character- glossus bicolor (Skinner 1973; Good 1995; Lobo et al. istic is probably related to the olfactory and chemosen- 1995, Hernandez et al. 2012). In Mabuya species the ba- sory ability, since Hernandez et al. (2012) observed that sicranial fenestra and pituitary fossa are still present in gimnophthalmids species with a large fenestra olfac- stage 40 D&H. However, in the preparturition stage, the toria have the main and accessory olfactory bulbs well pituitary fossa is closed and the basicranial fenestra are developed. closed or almost closed (similar to a slit). This is differ- The scaffolding in orbitotemporal region changes with ent from T. capensis where the pituitary fossa is closed in the body-plan, presenting reductions of some cartilages in the preparturition stage, but the basicranial fenestra is still serpentiform skinks like Lygosoma sp., Acontias melea- present in the juvenile stage. gris and Chalcides sepsoides (Pearson 1921; Bellaris & In relation to the dermatocranium, the development Kamal 1981). In lacertiform skinks, the scaffolding is ful- of bony elements starts in stage 33 with the differentia- ly developed, like C. ocellatus, P. fasciauts and T. capen- tion of the pterigoyd in Mabuya sp. and M. caissara, and sis (Rice 1920; El-Toubi & Kamal 1959; Skinner 1973); the pterigoyd and dentary in M. macrorhyncha (Table 2). this last characteristic is observed in M. cassaira, M. mac- Posteriorly, in stage 34, other bony elements start to os- rorhyncha and Mabuya sp. On the other hand, the pila sify (frontal, prefrontal, parietal, supratemporal, palatine, antotica is short and has no contact with the basal plate in dentary and surangular). Finally, in stage 40 (D&H), all Mabuya species (Table 1). This characteristic is observed elements are almost completely developed, except for in C. ocellatus, T. capensis and Lygosoma sp., while in the frontal and the parietal ones, which only show the P. fasciauts is absent (Pearson 1921; El-Toubi & Kamal margins. In the pre-parturition stage, the frontal and pa- 1959; Skinner 1973). In Mabuya species, the pila antotica rietal bones are almost fully differentiated; therefore, the is similar to that of T. capensis, which is short and only frontoparietal fenestra is small and remains open. Der- reaches the epipterigoyd position; however, during devel- matocranium development in Mabuya species is similar opment Mabuya species present differences with African to the other lizards and the pterygoids appear early, as T. capensis, since Skinner (1973) observed that the pila in Elgaria coerulea (Good 1995), Trachylepis capensis antotica is contacting the basal plate in stages 32 to 35 (Skinner 1973), and Liolaemus scapularis (Lobo et al. (D&H), this contact being lost in later stages. In Mabuya 1995). The other bony elements ossify early and corre- species the pila antotica has not been seen in contact with spond to the palatine, orbital and jaw region; this char- the basal plate during embryonic development. While we acteristic is observed in Trachylepis capensis (Skinner do not have other skink species for further embryonic 1973), Lacerta vivipara (Rieppel 1992), L. agilis (Riep- comparisons, it is nonetheless obvious that Mabuya spe- pel 1994) and Elgaria coerulea (Good 1995). We found cies are different in the development of pila antotica in re- that the entire ossification of parietal and frontal is ob- spect to T. capensis, thus indicating a difference between served in preparturing stages of Mabuya species, while in American and African clades in the development of this T. capensis it occurs in postnatal development (juvenile chondrocraneal characteristic. stage) (Skinner 1973). On the other hand, the vomer is On the other hand, the differentiation of the orbito- a paired bony element in Mabuya embryos, but in post- sphenoid, a semi-lunar ossification in the pila metoptica embrionary stage a distinctive bony element is formed by of the orbitotemporal region, is observed in the stage 40 fusion, this is a characteristic of adult stages of Mabuya (D&H) in Mabuya species (Table 1). In T. capensis it is sp. (Jerez 2012), while in African and Asiatic species the developed in postembryonic stages, appearing in adults vomer remains a paired bony element through their entire (Skinner 1973). A similar characteristic is probably pres- ontogeny. ent in Lygosoma sp., since the orbitosphenoid is not pres- Therefore, the skull development of the American ent in the fully formed chondrocranium of the embryo, Mabuya presents differences with Trachylepis capensis in but it is present in the adult stage (Rao & Ramaswami the development of pila antotica, the differentiation of the 1952). Therefore, the development of the orbitosphenoid orbitosphenoid, the closure of pituitary and basicranial fe- Acta Zool. Mex. (n.s.) 31(3) (2015) 401 nestrae, the ossification of parietal, and the development El-Toubi M. R. & Kamal, A. M. 1961. The development of the skull of vomer. Our evidences suggest that these characteris- of Ptyodactylus hasselquistii. I. The development of the chondro- tics should be regarded as diagnostic for Mabuya. There- cranium. Journal of Morphology, 108: 63-93. Fitzinger, L. J. 1843. Systema Reptilium. Fasciculus Primus. Amblyg- fore, these unique developmental patterns of Mabuya sp., lossae. Vienna: Braumuller et Seidel Biblipolas, Vindobonae. Mabuya caissara and M. macrorhyncha add weight to the Good D. A. 1995. Cranial ossification in the northern alligator Elgaria systematic hypothesis (Mausfeld et al. 2002), splitting the coerulea (Squamata, Anguidae). Amphibia-Reptilia, 16: 157-166. American genus Mabuya from the African genera Tra- Gray, J. E. 1845. Catalogue of the specimens of lizards in the collec- chylepis and Chioninia, and the Asian genus Chioninia. tion of the British Museum. London: The Trustees of the British Museum (Natural History). Greer, A. E., Arnold, C. & Arnold, E. N. 2000. The systematic sig- ACKNOWLEDGMENTS. We would like to thank the Colección nificance of the number of presacral vertebrae in the scincid lizard Herpetologica, Laboratorio de Biologia Reproductiva de Vertebrados, genus Mabuya. Amphibia-Reptilia, 21: 121-126. Universidad Industrial de Santander (Bucaramanga, Colombia) and Greer, A. E. & Nussbaum, R. A. 2000. A new character useful in the Museu de Zoología da Universidade de São Paulo (São Paulo, Bra- the systematics of the scincid lizard genus Mabuya. Copeia, 2000: zil) for allowing us to prepare the material examined. The first author 615-618. would like to thank Marissa Fabrezi (IBIOGEO, CONICET, Salta, Hedges, S. B. & Conn, C. E. 2012. A new skink fauna from Carib- Argentina) and Virginia Abdala (Universidad Nacional de Tucumán, bean islands (Squamata, Mabuyidae, Mabuyinae). Zootaxa, 3288: CONICET, Argentina) for her support and collaboration without whi- 1-244. ch the realization of this work would not have been possible. PMSM Hernández-Jaimes, C., Jerez, A. & Ramírez, M. P. 2012. Embry- and RAGF are grateful to H. 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